Comparison of oral microbiota in tumor and non-tumor tissues of patients with oral squamous cell carcinoma

Smruti Pushalkar, Xiaojie Ji, Yihong Li, Cherry Estilo, Ramanathan Yegnanarayana, Bhuvanesh Singh, Xin Li, Deepak Saxena, Smruti Pushalkar, Xiaojie Ji, Yihong Li, Cherry Estilo, Ramanathan Yegnanarayana, Bhuvanesh Singh, Xin Li, Deepak Saxena

Abstract

Background: Bacterial infections have been linked to malignancies due to their ability to induce chronic inflammation. We investigated the association of oral bacteria in oral squamous cell carcinoma (OSCC/tumor) tissues and compared with adjacent non-tumor mucosa sampled 5 cm distant from the same patient (n = 10). By using culture-independent 16S rRNA approaches, denaturing gradient gel electrophoresis (DGGE) and cloning and sequencing, we assessed the total bacterial diversity in these clinical samples.

Results: DGGE fingerprints showed variations in the band intensity profiles within non-tumor and tumor tissues of the same patient and among the two groups. The clonal analysis indicated that from a total of 1200 sequences characterized, 80 bacterial species/phylotypes were detected representing six phyla, Firmicutes, Bacteroidetes, Proteobacteria, Fusobacteria, Actinobacteria and uncultivated TM7 in non-tumor and tumor libraries. In combined library, 12 classes, 16 order, 26 families and 40 genera were observed. Bacterial species, Streptococcus sp. oral taxon 058, Peptostreptococcus stomatis, Streptococcus salivarius, Streptococcus gordonii, Gemella haemolysans, Gemella morbillorum, Johnsonella ignava and Streptococcus parasanguinis I were highly associated with tumor site where as Granulicatella adiacens was prevalent at non-tumor site. Streptococcus intermedius was present in 70% of both non-tumor and tumor sites.

Conclusions: The underlying changes in the bacterial diversity in the oral mucosal tissues from non-tumor and tumor sites of OSCC subjects indicated a shift in bacterial colonization. These most prevalent or unique bacterial species/phylotypes present in tumor tissues may be associated with OSCC and needs to be further investigated with a larger sample size.

Figures

Figure 1
Figure 1
DGGE profile of microbial communities from two clinically distinct non-tumor and tumor groups. N–Non-tumor; T–Tumor; Marker I & II: DGGE reference markers correspond to 16S rRNA gene fragments from quoted specific bacterial species [Marker I: 1. Fusobacterium nucleatum subsp. vincenti (ATCC 49256); 2. Fusobacterium nucleatum subsp. nucleatum (ATCC 25586); 3. Streptococcus sanguinis (ATCC 10556); 4. Streptococcus oralis (ATCC 35037); 5. Streptococcus salivarius (ATCC 7073); 6. Streptococcus mutans (UA 159); 7. Lactobacillus paracasei (ATCC 25598); 8. Porphyromonas gingivalis (ATCC 33277); 9. Actinomyces odontolyticus (ATCC 17929);10. Actinomyces naeslundii (ATCC 12104), Marker II: 1. F. nucleatum subsp. vincenti (ATCC 49256); 2. F. nucleatum subsp. nucleatum (ATCC 25586); 3. Bacteroides forsythus (ATCC 43037); 4. S. sanguinis (ATCC 10556); 5. S. oralis (ATCC 35037); 6. Veillonella parvula (ATCC 17745); 7. Prevotella intermedia (ATCC 25611); 8. Aggregatibacter actinomycemcomitans (ATCC 43717); 9. P. gingivalis (ATCC 33277); 10. A.odontolyticus (ATCC 17929); 11. A. naeslundii (ATCC 12104)].
Figure 2
Figure 2
Dendrogram representing the fingerprinting intensity profile of two clinically distinct samples from non-tumor and tumor tissues. N–Non-tumor; T–Tumor.
Figure 3
Figure 3
Distribution of relative abundance of phyla in (a) Individual sample set, non-tumor and tumor sites of each OSCC patient and; (b) Cumulative non-tumor and tumor libraries, as detected by HOMD and RDP. N–Non-tumor; T–Tumor.
Figure 4
Figure 4
Distribution of relative abundance of genera at (a) Non-tumor and tumor sites of each OSCC subject; and (b) Cumulative non-tumor and tumor libraries, as detected by HOMD and RDP; (c) Pie-chart shows the relative prevalence of gram-negative and gram-positive bacteria and venn diagram depicts the genera in tissue samples of OSCC subjects.*p < 0.1. N–Non-tumor; T–Tumor. Pie-chart shows the relative shift of gram-negative and gram-positive microbiota in non-tumor and tumor tissue samples. Values in the venn diagram represent the genera shared by and exclusive to non-tumor and tumor tissue libraries.
Figure 5
Figure 5
Relative distribution of total bacteria (cultivable species and uncultured phylotypes) in tissues from non-tumor and tumor sites of OSCC subjects characterized by HOMD. Core of pie chart shows percentage distribution of total 914 filtered sequences in terms of their % homology to curated 16S rRNA sequences in HOMD. Outer concentric of pie chart depicts the oral bacterial taxa in combined library; sequences with >98% identity: named cultured species (78.6%), unnamed cultured species (5.9%) and yet-uncultured phylotypes (3.8%); and sequences with <98% identity (11.7%) were considered as unclassified sequences characterized only to genus level. Venn diagrams correlates with the corresponding section of pie chart as indicated by line except for the unclassified sequences. Inset values in two subsets (non-tumor and tumor) represents observed bacterial species unique to that particular library. Values in overlapping section of subsets reflect oral taxa common to both sites.
Figure 6
Figure 6
Prevalence of bacterial species/phylotypes associated with non-tumor and tumor sites of OSCC subjects corresponding to phyla: (a) Bacteroidetes, Proteobacteria, Fusobacteria, Actinobacteria, uncultured TM7; and (b) Firmicutes, as detected by HOMD.

References

    1. Bagan J, Sarrion G, Jimenez Y. Oral cancer: clinical features. Oral Oncol. 2010;46(6):414–417. doi: 10.1016/j.oraloncology.2010.03.009.
    1. Rosenquist K. Risk factors in oral and oropharyngeal squamous cell carcinoma: a population-based case-control study in southern Sweden. Swed Dent J Suppl. 2005;179:1–66.
    1. Scully C, Bagan J. Oral squamous cell carcinoma: overview of current understanding of aetiopathogenesis and clinical implications. Oral Dis. 2009;15(6):388–399. doi: 10.1111/j.1601-0825.2009.01563.x.
    1. Altekruse SF KC, Krapcho M, Neyman N, Aminou R, Waldron W, Ruhl J, Howlader N, Tatalovich Z, Cho H, editor. SEER Cancer Statistics Review, 1975-2008. Bethesda, MD: National Cancer Institute; 1975-2008. posted to the SEER web site, 2011, based on November 2010 SEER data submission.
    1. Johnson NW, Jayasekara P, Amarasinghe AAHK. Squamous cell carcinoma and precursor lesions of the oral cavity: epidemiology and aetiology. Periodontol. 2011;57(1):19–37. doi: 10.1111/j.1600-0757.2011.00401.x.
    1. Tanaka T, Tanaka M, Tanaka T. Oral carcinogenesis and oral cancer chemoprevention: a review. Pathol Res Int 2011. 2011. p. 10 pages. Article ID 431246.
    1. Tsantoulis PK, Kastrinakis NG, Tourvas AD, Laskaris G, Gorgoulis VG. Advances in the biology of oral cancer. Oral Oncol. 2007;43(6):523–534. doi: 10.1016/j.oraloncology.2006.11.010.
    1. Lax AJ, Thomas W. How bacteria could cause cancer: one step at a time. Trends Microbiol. 2002;10(6):293–299. doi: 10.1016/S0966-842X(02)02360-0.
    1. Pujol FH, Devesa M. Genotypic variability of hepatitis viruses associated with chronic infection and the development of hepatocellular carcinoma. J Clin Gastroenterol. 2005;39(7):611–618. doi: 10.1097/01.mcg.0000170770.49394.92.
    1. Nagy KN, Sonkodi I, Szoke I, Nagy E, Newman HN. The microflora associated with human oral carcinomas. Oral Oncol. 1998;34(4):304–308.
    1. Sharma Mohit Bairy I, Pai K, Satyamoorthy K, Prasad S, Berkovitz B, Radhakrishnan R. Salivary IL-6 levels in oral leukoplakia with dysplasia and its clinical relevance to tobacco habits and periodontitis. Clin Oral Invest. 2010;15(5):705–714.
    1. Tezal M, Sullivan MA, Hyland A, Marshall JR, Stoler D, Reid ME, Loree TR, Rigual NR, Merzianu M, Hauck L. et al.Chronic periodontitis and the incidence of head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 2009;18(9):2406–2412. doi: 10.1158/1055-9965.EPI-09-0334.
    1. Lissowska J, Pilarska A, Pilarski P, Samolczyk-Wanyura D, Piekarczyk J, Bardin-Mikollajczak A, Zatonski W, Herrero R, Munoz N. et al.Smoking, alcohol, diet, dentition and sexual practices in the epidemiology of oral cancer in Poland. Eur J Cancer Prev. 2003;12(1):25–33. doi: 10.1097/00008469-200302000-00005.
    1. Hooper SJ, Wilson MJ, Crean SJ. Exploring the link between microorganisms and oral cancer: a systematic review of the literature. Head Neck. 2009;31(9):1228–1239. doi: 10.1002/hed.21140.
    1. Lax AJ. Opinion: bacterial toxins and cancer-a case to answer? Nat Rev Microbiol. 2005;3(4):343–349. doi: 10.1038/nrmicro1130.
    1. Mantovani A, Garlanda C, Allavena P. Molecular pathways and targets in cancer-related inflammation. Ann Med. 2010;42(3):161–170. doi: 10.3109/07853890903405753.
    1. Meurman J. Oral microbiota and cancer. J Oral Microbiol. 2010;2:5195. doi: 10.3402/jom.v2i0.5195.
    1. Tsai HF, Hsu PN. Interplay between Helicobacter pylori and immune cells in immune pathogenesis of gastric inflammation and mucosal pathology. Cell Mol Immunol. 2010;7(4):255–259. doi: 10.1038/cmi.2010.2.
    1. Mager DL. Bacteria and cancer: cause, coincidence or cure? a revie. J Transl Med. 2006;4:14. doi: 10.1186/1479-5876-4-14.
    1. Vogelmann R, Amieva MR. The role of bacterial pathogens in cancer. Curr Opin Microbiol. 2007;10(1):76–81. doi: 10.1016/j.mib.2006.12.004.
    1. Ward JM, Fox JG, Anver MR, Haines DC, George CV, Collins MJ Jr, Gorelick PL, Nagashima K, Gonda MA, Gilden RV. et al.Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J Natl Cancer Inst. 1994;86(16):1222–1227. doi: 10.1093/jnci/86.16.1222.
    1. Engle SJ, Ormsby I, Pawlowski S, Boivin GP, Croft J, Balish E, Doetschman T. Elimination of colon cancer in germ-free transforming growth factor beta 1-deficient mice. Cancer Res. 2002;62(22):6362–6366.
    1. Rao VP, Poutahidis T, Fox JG, Erdman SE. Breast cancer: should gastrointestinal bacteria be on our radar screen? Cancer Res. 2007;67(3):847–850. doi: 10.1158/0008-5472.CAN-06-3468.
    1. Kuper H, Adami HO, Trichopoulos D. Infections as a major preventable cause of human cancer. J Int Med. 2000;248:171–183. doi: 10.1046/j.1365-2796.2000.00742.x.
    1. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860–867. doi: 10.1038/nature01322.
    1. Eskan MA, Hajishengallis G, Kinane DF. Differential activation of human gingival epithelial cells and monocytes by Porphyromonas gingivalis fimbriae. Infect Immun. 2007;75(2):892–898. doi: 10.1128/IAI.01604-06.
    1. Fukata M, Hernandez Y, Conduah D, Cohen J, Chen A, Breglio K, Goo T, Hsu D, Xu R, Abreu MT. Innate immune signaling by Toll-like receptor-4 (TLR4) shapes the inflammatory microenvironment in colitis-associated tumors. Inflamm Bowel Dis. 2009;15(7):997–1006. doi: 10.1002/ibd.20880.
    1. Califano J, van der Riet P, Westra W, Nawroz H, Clayman G, Piantadosi S, Corio R, Lee D, Greenberg B, Koch W. et al.Genetic progression model for head and neck cancer: implications for field cancerization. Cancer Res. 1996;56(11):2488–2492.
    1. Chen Z, Malhotra PS, Thomas GR, Ondrey FG, Duffey DC, Smith CW, Enamorado I, Yeh NT, Kroog GS, Rudy S. et al.Expression of proinflammatory and proangiogenic cytokines in human head and neck cancer patients. Head Neck. 1998;20:450.
    1. De Schutter H, Landuyt W, Verbeken E, Goethals L, Hermans R, Nuyts S. The prognostic value of the hypoxia markers CA IX and GLUT 1 and the cytokines VEGF and IL 6 in head and neck squamous cell carcinoma treated by radiotherapy ± chemotherapy. BMC Cancer. 2005;5:42. doi: 10.1186/1471-2407-5-42.
    1. Rhodus NL, Ho V, Miller CS, Myers S, Ondrey F. NF-kappaB dependent cytokine levels in saliva of patients with oral preneoplastic lesions and oral squamous cell carcinoma. Cancer Detect Prev. 2005;29(1):42–45. doi: 10.1016/j.cdp.2004.10.003.
    1. Kroes I, Lepp PW, Relman DA. Bacterial diversity within the human subgingival crevice. PNAS. 1999;96(25):14547–14552. doi: 10.1073/pnas.96.25.14547.
    1. Nagy K, Szoke I, Sonkodi I, Nagy E, Mari A, Szolnoky G, Newman HN. Inhibition of microflora associated with oral malignancy. Oral Oncol. 2000;36(1):32–36. doi: 10.1016/S1368-8375(99)00046-9.
    1. Hooper SJ, Crean SJ, Lewis MA, Spratt DA, Wade WG, Wilson MJ. Viable bacteria present within oral squamous cell carcinoma tissue. J Clin Microbiol. 2006;44(5):1719–1725. doi: 10.1128/JCM.44.5.1719-1725.2006.
    1. Sakamoto H, Sasaki J, Nord CE. Association between bacterial colonization on the tumor, bacterial translocation to the cervical lymph nodes and subsequent postoperative infection in patients with oral cancer. Clin Microbiol Infect. 1999;5(10):612–616. doi: 10.1111/j.1469-0691.1999.tb00417.x.
    1. Sasaki M, Yamaura C, Ohara-Nemoto Y, Tajika S, Kodama Y, Ohya T, Harada R, Kimura S. Streptococcus anginosus infection in oral cancer and its infection route. Oral Dis. 2005;11(3):151–156. doi: 10.1111/j.1601-0825.2005.01051.x.
    1. Ahn J, Yang L, Paster BJ, Ganly I, Morris L, Pei Z, Hayes RB. Oral microbiome profiles: 16S rRNA pyrosequencing and microarray assay comparison. PLoS One. 2011;6(7):e22788. doi: 10.1371/journal.pone.0022788.
    1. Hooper SJ, Crean SJ, Fardy MJ, Lewis MA, Spratt DA, Wade WG, Wilson MJ. A molecular analysis of the bacteria present within oral squamous cell carcinoma. J Med Microbiol. 2007;56(12):1651–1659. doi: 10.1099/jmm.0.46918-0.
    1. Mager DL, Haffajee AD, Devlin PM, Norris CM, Posner MR, Goodson JM. The salivary microbiota as a diagnostic indicator of oral cancer: a descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. J Transl Med. 2005;3:27. doi: 10.1186/1479-5876-3-27.
    1. Pushalkar S, Mane SP, Ji X, Li Y, Evans C, Crasta OR, Morse D, Meagher R, Singh A, Saxena D. Microbial diversity in saliva of oral squamous cell carcinoma. FEMS Immunol Med Microbiol. 2011;61(3):269–277. doi: 10.1111/j.1574-695X.2010.00773.x.
    1. Estilo C, O-charoenrat P, Talbot S, Socci N, Carlson D, Ghossein R, Williams T, Yonekawa Y, Ramanathan Y, Boyle J. et al.Oral tongue cancer gene expression profiling: identification of novel potential prognosticators by oligonucleotide microarray analysis. BMC Cancer. 2009;9(1):11. doi: 10.1186/1471-2407-9-11.
    1. Estilo CL, O-charoenrat P, Ngai I, Patel SG, Reddy PG, Dao S, Shaha AR, Kraus DH, Boyle JO, Wong RJ. et al.The role of novel oncogenes squamous cell carcinoma-related oncogene and phosphatidylinositol 3-kinase p110alpha in squamous cell carcinoma of the oral tongue. Clin Cancer Res. 2003;9(6):2300–2306.
    1. Singh B, Reddy PG, Goberdhan A, Walsh C, Dao S, Ngai I, Chou TC, O-charoenrat P, Levine AJ, Rao PH. et al.p53 regulates cell survival by inhibiting PIK3CA in squamous cell carcinomas. Genes Dev. 2002;16(8):984–993. doi: 10.1101/gad.973602.
    1. Ji X, Pushalkar S, Li Y, Glickman R, Fleisher K, Saxena D. Antibiotic effects on bacterial profile in osteonecrosis of the jaw. Oral Dis. 2012;18(1):85–95. doi: 10.1111/j.1601-0825.2011.01848.x.
    1. Li Y, Ge Y, Saxena D, Caufield PW. Genetic profiling of the oral microbiota associated with severe early-childhood caries. J Clin Microbiol. 2007;45(1):81–87. doi: 10.1128/JCM.01622-06.
    1. Eden PA, Schmidt TM, Blakemore RP, Pace NR. Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-Specific DNA. Int J Syst Bacteriol. 1991;41(2):324–325. doi: 10.1099/00207713-41-2-324.
    1. Gee JE, Sacchi CT, Glass MB, De BK, Weyant RS, Levett PN, Whitney AM, Hoffmaster AR, Popovic T. Use of 16S rRNA gene sequencing for rapid identification and differentiation of Burkholderia pseudomallei and B. mallei. J Clin Microbiol. 2003;41(10):4647–4654. doi: 10.1128/JCM.41.10.4647-4654.2003.
    1. Lane D. In: Nucleic acid techniques in bacterial systematics. Stackebrandt E, Goodfellow M, editor. John Wiley & Sons Ltd, West Sussex; 1991. 16S/23S rRNA sequencing; pp. 115–147.
    1. Rupf S, Merte K, Eschrich K. Quantification of bacteria in oral samples by competitive polymerase chain reaction. J Dent Res. 1999;78(4):850–856. doi: 10.1177/00220345990780040501.
    1. Zoetendal EG, Akkermans ADL, De Vos WM. Temperature gradient gel electrophoresis analysis of 16s rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol. 1998;64(10):3854–3859.
    1. Li Y, Ku CY, Xu J, Saxena D, Caufield PW. Survey of oral microbial diversity using PCR-based denaturing gradient gel electrophoresis. J Dent Res. 2005;84(6):559–564. doi: 10.1177/154405910508400614.
    1. Li Y, Saxena D, Barnes VM, Trivedi HM, Ge Y, Xu T. Polymerase chain reaction-based denaturing gradient gel electrophoresis in the evaluation of oral microbiota. Oral Microbiol Immunol. 2006;21(5):333–339. doi: 10.1111/j.1399-302X.2006.00301.x.
    1. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R. et al.Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947–2948. doi: 10.1093/bioinformatics/btm404.
    1. DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 2006;34:W394–W399. doi: 10.1093/nar/gkl244.
    1. Huber T, Faulkner G, Hugenholtz P. Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics. 2004;20:2317–2319. doi: 10.1093/bioinformatics/bth226.
    1. Chen T, Yu W-H, Izard J, Baranova OV, Lakshmanan A, Dewhirst FE. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database. 2010. Article ID baq013.
    1. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner ACR, Yu W-H, Lakshmanan A, Wade WG. The human oral microbiome. J Bacteriol. 2010;192(19):5002–5017. doi: 10.1128/JB.00542-10.
    1. Tanner ACR, Mathney JMJ, Kent RL, Chalmers NI, Hughes CV, Loo CY, Pradhan N, Kanasi E, Hwang J, Dahlan MA. et al.Cultivable anaerobic microbiota of severe early childhood caries. J Clin Microbiol. 2011;49(4):1464–1474. doi: 10.1128/JCM.02427-10.
    1. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM. et al.The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009;37:D141–145. doi: 10.1093/nar/gkn879.
    1. Colwell RK. EstimateS: statistical estimation of species richness and shared species from samples. Version 8.2. 2009. User's guide and application published at: .
    1. Hammer O, Harper D, Ryan P. PAST: palaeontological statistics software package for education and data analysis. Palaeontol Electron. 2001;4:1–9.
    1. Good I. The population frequencies of species and the estimation of population parameters. Biometrika. 1953;40:237–264.
    1. Bebek G, Bennett KL, Funchain P, Campbell R, Seth R, Scharpf J, Burkey B, Eng C. Microbiomic subprofiles and MDR1 promoter methylation in head and neck squamous cell carcinoma. Hum Mol Genet. 2011;21(7):1557–1565.
    1. Katz J, Onate MD, Pauley KM, Bhattacharyya I, Cha S. Presence of Porphyromonas gingivalis in gingival squamous cell carcinoma. Int J Oral Sci. 2011;3(4):209–215. doi: 10.4248/IJOS11075.
    1. Hayashi C, Gudino CV, Gibson FC III, Genco CA. Pathogen-induced inflammation at sites distant from oral infection: bacterial persistence and induction of cell-specific innate immune inflammatory pathways. Mol Oral Microbiol. 2010;25(5):305–316. doi: 10.1111/j.2041-1014.2010.00582.x.
    1. Lerman LS, Fischer SG, Hurley I, Silverstein K, Lumelsky N. Sequence-determined DNA separations. Annu Rev Biophys Bioeng. 1984;13:399–423. doi: 10.1146/annurev.bb.13.060184.002151.
    1. Ercolini D. PCR-DGGE fingerprinting: novel strategies for detection of microbes in food. J Microbiol Methods. 2004;56(3):297–314. doi: 10.1016/j.mimet.2003.11.006.
    1. Rocas IN, Siqueira JF Jr, Aboim MC, Rosado AS. Denaturing gradient gel electrophoresis analysis of bacterial communities associated with failed endodontic treatment. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2004;98(6):741–749. doi: 10.1016/j.tripleo.2004.09.006.
    1. Zaura E, Keijser BJ, Huse SM, Crielaard W. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol. 2009;9:259. doi: 10.1186/1471-2180-9-259.
    1. Siqueira JF, Rocas IN. Uncultivated phylotypes and newly named species associated with primary and persistent endodontic infections. J Clin Microbiol. 2005;43(7):3314–3319. doi: 10.1128/JCM.43.7.3314-3319.2005.
    1. Eribe ER, Olsen I. Leptotrichia species in human infections. Anaerobe. 2008;14(3):131–137. doi: 10.1016/j.anaerobe.2008.04.004.
    1. Ruoff KL. Miscellaneous catalase-negative, gram-positive cocci: emerging opportunists. J Clin Microbiol. 2002;40(4):1129–1133. doi: 10.1128/JCM.40.4.1129-1133.2002.
    1. Carlier J-P, K'ouas G, Bonne I, Lozniewski A, Mory F. Oribacterium sinus gen. nov., sp. nov., within the family ‘Lachnospiraceae’ (phylum Firmicutes) Int J Syst Evol Microbiol. 2004;54(5):1611–1615. doi: 10.1099/ijs.0.63060-0.
    1. Morita E, Narikiyo M, Yokoyama A, Yano A, Kamoi K, Yoshikawa E, Yamaguchi T, Igaki H, Tachimori Y, Kato H. et al.Predominant presence of Streptococcus anginosus in the saliva of alcoholics. Oral Microbiol Immunol. 2005;20(6):362–365. doi: 10.1111/j.1399-302X.2005.00242.x.
    1. Gray T. Streptococcus anginosus group: clinical significance of an important group of pathogens. Clin Microbiol Newsl. 2005;27(20):155–159. doi: 10.1016/j.clinmicnews.2005.09.006.
    1. Nakazawa F, Miyakawa H, Fujita M, Kamaguchi A. Significance of asaccharolytic Eubacterium and closely related bacterial species in the human oral cavity. J Expt Clin Med. 2011;3(1):17–21. doi: 10.1016/j.jecm.2010.12.008.
    1. Colombo APV, Teles RP, Torres MC, Souto R, Rosalém W, Mendes MCS, Uzeda M. Subgingival microbiota of brazilian subjects with untreated chronic periodontitis. J Periodontol. 2002;73(4):360–369. doi: 10.1902/jop.2002.73.4.360.
    1. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA, Sahasrabudhe A, Dewhirst FE. Bacterial diversity in human subgingival plaque. J Bacteriol. 2001;183(12):3770–3783. doi: 10.1128/JB.183.12.3770-3783.2001.
    1. Fitzpatrick SG, Katz J. The association between periodontal disease and cancer: a review of the literature. J Dent. 2010;38(2):83–95. doi: 10.1016/j.jdent.2009.10.007.
    1. Kumagai K, Sugano N, Takane M, Iwasaki H, Tanaka H, Yoshinuma N, Suzuki K, Ito K. Detection of Streptococcus anginosus from saliva by real-time polymerase chain reaction. Lett Appl Microbiol. 2003;37(5):370–373. doi: 10.1046/j.1472-765X.2003.01405.x.
    1. van Houte J, Lopman J, Kent R. The final pH of bacteria comprising the predominant flora on sound and carious human root and enamel surfaces. J Dent Res. 1996;75:1008–1014. doi: 10.1177/00220345960750040201.
    1. van Houte J, Sansone C, Joshipura K, Kent R. Mutans streptococci and non- mutans streptococci acidogenic at low pH, and in vitro acidogenic potential of dental plaque in two different areas of the human dentition. J Dent Res. 1991;70:1503–1507. doi: 10.1177/00220345910700120601.
    1. Beighton D. The complex oral microflora of high-risk individuals and groups and its role in the caries process. Community Dent Oral Epidemiol. 2005;33(4):248–255. doi: 10.1111/j.1600-0528.2005.00232.x.
    1. Downes J, Wade WG. Peptostreptococcus stomatis sp. nov., isolated from the human oral cavity. Int J Syst Evol Microb. 2006;56(4):751–754. doi: 10.1099/ijs.0.64041-0.
    1. Lunt SJ, Chaudary N, Hill RP. The tumor microenvironment and metastatic disease. Clin Exp Metastasis. 2009;26(1):19–34. doi: 10.1007/s10585-008-9182-2.
    1. Mazzio E, Smith B, Soliman K. Evaluation of endogenous acidic metabolic products associated with carbohydrate metabolism in tumor cells. Cell Biol Toxicol. 2010;26(3):177–188. doi: 10.1007/s10565-009-9138-6.
    1. Collins MD, Hutson RA, Falsen E, Sjoden B, Facklam RR. Description of Gemella sanguinis sp. nov., isolated from human clinical specimens. J Clin Microbiol. 1998;36(10):3090–3093.
    1. Willems A, Collins MD. Evidence for the placement of the gram-negative Catonella morbi (Moore and Moore) and Johnsonella ignava (Moore and Moore) within the Clostridium subphylum of the gram-positive bacteria on the basis of 16S rRNA sequences. Int J Syst Bacteriol. 1995;45(4):855–857. doi: 10.1099/00207713-45-4-855.
    1. Michaud DS, Liu Y, Meyer M, Giovannucci E, Joshipura K. Periodontal disease, tooth loss, and cancer risk in male health professionals: a prospective cohort study. Lancet Oncol. 2008;9(6):550–558. doi: 10.1016/S1470-2045(08)70106-2.
    1. Rosenquist K, Wennerberg J, Schildt EB, Bladström A, Göran Hansson B, Andersson G. Oral status, oral infections and some lifestyle factors as risk factors for oral and oropharyngeal squamous cell carcinoma. A population-based case-control study in southern Sweden. Acta Otolaryngol. 2005;125(12):1327–1. doi: 10.1080/00016480510012273.
    1. Tezal M, Sullivan MA, Reid ME, Marshall JR, Hyland A, Loree T, Lillis C, Hauck L, Wactawski-Wende J, Scannapieco FA. Chronic periodontitis and the risk of tongue cancer. Arch Otolaryngol Head Neck Surg. 2007;133(5):450–454. doi: 10.1001/archotol.133.5.450.
    1. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol. 2005;43(11):5721–5732. doi: 10.1128/JCM.43.11.5721-5732.2005.
    1. Mager DL, Ximenez-Fyvie LA, Haffajee AD, Socransky SS. Distribution of selected bacterial species on intraoral surfaces. J Clin Periodontol. 2003;30(7):644–654. doi: 10.1034/j.1600-051X.2003.00376.x.
    1. Allavena P, Garlanda C, Borrello MG, Sica A, Mantovani A. Pathways connecting inflammation and cancer. Curr Opin Genet Dev. 2008;18(1):3–10. doi: 10.1016/j.gde.2008.01.003.
    1. Kurago Z, Lam-ubol A, Stetsenko A, De La Mater C, Chen Y, Dawson D. Lipopolysaccharide-Squamous Cell Carcinoma-Monocyte interactions induce cancer-supporting factors leading to rapid STAT3 activation. Head Neck Pathol. 2008;2(1):1–12. doi: 10.1007/s12105-007-0038-x.
    1. Berezow AB, Darveau RP. Microbial shift and periodontitis. Periodontol. 2011;55(1):36–47. doi: 10.1111/j.1600-0757.2010.00350.x.

Source: PubMed

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